Plant Growth Regulation

, Volume 29, Issue 1–2, pp 47–76 | Cite as

Molecular analysis of acclimation to cold

  • Roger S. Pearce


Temperature is expected to affect all plant processes. Consistent with this, expression of a large number of specific mRNAs and proteins is up-regulated during cold-acclimation. Their possible functions are outlined, encompassing a wide range of processes, some possibly related to other winter stresses besides cold. Some of the cold-responsive sequences are associated with constitutive or stress-related metabolism, others are probably protective, some may influence freezing, and many are of as yet unknown function. While many of the sequences code for intracellular proteins, a significant number code for apoplastic proteins with a variety of possible functions. Transient influx of calcium into the cytosol appears to be a key step in the response to cold, and also to many other stresses and signals. Similarly, the cold-responsive promoter element identified so far is also responsive to drought and salt. However, how cold is sensed, and any cold-specific aspects of the cold signal transduction pathway, are, so far, unknown. What is clear is that, at least in the model plant Arabidopsis thaliana, cold-, desiccation-, salt- and ABA-triggered signal transduction pathways, and possibly others, run partly in parallel and partly intersect. This may be partly explained by a need for an integrated winter-response. The total number of genes which are cold-responsive and the quantity of resources which this implies are used in this way, indicate that many must have a positive role in acclimation. Experiments which modify membrane lipid unsaturation or solute accumulation, achieved by transformation of plants to express exotic or heterologous genes or by other means, confirm that these factors affect chill- or freezing-tolerance. A transgenic test has shown that one cold-up-regulated gene of previously unknown function contributes to freezing-tolerance, but the small effect re-emphasises the probably cumulative nature of the contributions of many cold-up-regulated sequences to acclimation. On the other hand, mutant analysis indicates some genes may make a comparatively larger contribution. Transformation of alfalfa to overexpress a superoxide dismutase gene increased cold-tolerance and drought-resistance and demonstrated that improvements in field-survival of stresses is possible by transgenic means. Over-expression of a transcription factor, CBF1, conferred freezing-tolerance on Arabidopsis, showing that manipulation of the signal transduction pathway could be an important method for modifying cold-tolerance.

cold chill freezing gene expression signal transduction pathways 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Aloni R and Griffiths M (1991) Functional xylem anatomy in root-shoot junctions of six cereal species. Planta 184: 123–129Google Scholar
  2. 2.
    Anderson JA, Gusta LV, Buchanan DW and Burke MJ (1983) Freezing of water in citrus leaves. J Am Soc Hort Sci 108: 397–400Google Scholar
  3. 3.
    Anderson JV, Li Q-B, Haskell DW and Guy CL (1994) Structural organization of the spinach endoplasmic reticulum-luminal 70 kilodalton heat-shock cognate gene and expression of 70 kilodalton heat-shock genes during cold acclimation. Plant Physiol 104: 1359–1370Google Scholar
  4. 4.
    Antikainen M and Griffith M (1997) Antifreeze protein accumulation in freezing-tolerant cereals. Physiol Plant 99: 423–432Google Scholar
  5. 5.
    Arakawa T and Timasheff SN (1985) The stabilization of proteins by osmolytes. Biophys J 47: 411–414Google Scholar
  6. 6.
    Arora R, Rowland LJ and Panta GR (1997) Chill-responsive dehydrins in blueberry: Are they associated with cold hardiness or dormancy transitions? Physiol Plant 101: 8–16Google Scholar
  7. 7.
    Arora R and Wisniewski ME (1994) Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch). Plant Physiol 105: 95–101Google Scholar
  8. 8.
    Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin CT and Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana cor15a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci USA 93: 13404–13409Google Scholar
  9. 9.
    Asghar R, Fenton RD, DeMason DA and Close TJ (1994) Nuclear and cytoplasmic localisation of maize embryo and aleurone dehydrin. Protoplasma 177: 87–94Google Scholar
  10. 10.
    Ashworth EN (1982) Properties of peach flower buds which facilitate supercooling. Plant Physiol 70: 1475–1479Google Scholar
  11. 11.
    Ashworth EN (1990) The formation and distribution of ice within forsythia flower buds. Plant Physiol 92: 718–725Google Scholar
  12. 12.
    Ashworth EN and Abeles FA (1984) Freezing behaviour of water in small pores and the possible role in the freezing of plant tissues. Plant Physiol 76: 201–204Google Scholar
  13. 13.
    Ashworth EN, Davis GA and Wisniewski ME (1989) The formation and distribution of ice within dormant and deacclimated peach flower buds. Plant Cell Envir 12: 521–528Google Scholar
  14. 14.
    Ashworth EN, Echlin P, Pearce RS and Hayes TL (1988) Ice formation and tissue response in apple twigs. Plant Cell Envir 11: 703–710Google Scholar
  15. 15.
    Ashworth EN, Wilard TJ and Malone SR (1992) The relationship between vascular differentiation and the distribution of ice within Forsythia flower buds. Plant Cell Envir 15: 607–612Google Scholar
  16. 16.
    Atherton KM (1997) Molecular and Physiological Analysis of Plant Cold Acclimation. PhD thesis, University of Newcastle upon TyneGoogle Scholar
  17. 17.
    Baker JC, Steele C and Dure L III (1988) Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol Biol 11: 277–291Google Scholar
  18. 18.
    Baertlein DA, Lindow SE, Panopoulos NJ, Lee SP, Mindrinos MN and Chen THH (1992) Expression of a bacterial ice nucleation gene in plants. Plant Physiol 100: 1730–1736Google Scholar
  19. 19.
    Baudo MM, Mezazepeda LA, Palva Et and Heino P (1996) Induction of homologous low-temperature and ABAresponsive genes in frost resistant (Solanum commersonii) and frost-sensitive (Solanum tuberosum cv Bintje) potato species. Plant Mol Biol 30: 331–336Google Scholar
  20. 20.
    Berberich T, Harda M, Sugawara K, Kodama H, Iba K and Kusano T (1998) Two maize genes encoding ω-3 fatty acid desaturas and their differential expression to temperature. Plant Mol Biol 36: 297–306Google Scholar
  21. 21.
    Berberich T, Suguwara K, Harada M and Kusano T (1995) Molecular cloning, characterisation and expression of an elongation factor 1-alpha gene in maize. Plant Mol Biol 29: 611–615Google Scholar
  22. 22.
    Boothe JG, Sonnichsen FD, deBeus FD and Johnson-Flanagan (1997) Purification, characterization, and structural analysis of a plant low-temperature-induced protein. Plant Physiol 113: 367–376Google Scholar
  23. 23.
    Boyer JS (1995) Biochemical and biophysical aspects of water deficits and the predisposition to disease. Annu Rev Phytopath 33: 251–274Google Scholar
  24. 24.
    Brandts JG, Fu J and Nordin JH (1970) The low temperature denaturation of chymotrypsinogen in aqueous solution and in frozen aqueous solution. In: Wolstenholme GEW and O'Connor MJ (eds) The Frozen Cell. London: Churchill, pp 189–212Google Scholar
  25. 25.
    Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103: 1035–1040Google Scholar
  26. 26.
    Bridger GM, Yang W, Falk DE and McKersie BD (1994) Cold-acclimation increases tolerance of activated oxygen in winter cereals. J Plant Physiol 144: 235–240Google Scholar
  27. 27.
    Brush RA, Griffith M and Mlynarz A (1994) Characterisation and quantification of intrinsic ice nucleators in winter rye (Secale cereale) leaves. Plant Physiol 104: 725–735Google Scholar
  28. 28.
    Burke MJ, Gusta LV, Quamme HA, Weiser CJ and Li PH (1976) Freezing and injury in plants. Annu Rev Plant Physiol 27: 507–528Google Scholar
  29. 29.
    Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46: 95–122Google Scholar
  30. 30.
    Cai GY, Moore GA and Guy CL (1995) Unusual group-2 LEA gene family in Citrus responsive to low-temperature. Plant Mol Biol 29: 11–23Google Scholar
  31. 31.
    Carpenter JF and Crowe JH (1988) The mechanism of cryoprotection of proteins by solutes. Cryobiology 25: 244–255Google Scholar
  32. 32.
    Carpenter CD, Krebs JA and Simon AE (1994) Genes encoding glycine-rich Arabidopsis thaliana proteins with RNA-binding motifs are influenced by cold treatment and an endogenous circadian rhythm. Plant Physiol 104: 1015–1025Google Scholar
  33. 33.
    Carystinos GD, Macdonald HR, Monroy AF, Dhindsa RS and Poole RJ (1995) Vacuolar H+-translocating pyrophosphatase is induced by anoxia or chilling in seedlings of rice. Plant Physiol 108: 641–649Google Scholar
  34. 34.
    Castonguay Y, Laberge S, Nadeau P and Vezina L-P (1994) A cold-induced gene from Medicago sativa encodes a bimodular protein similar to developmentally-regulated proteins. Plant Mol Biol 24: 799–804Google Scholar
  35. 35.
    Chalker-Scott L (1992) Disruption of an ice-nucleation barrier in cold hardy Azalea buds by sublethal heat stress. Ann Bot 70: 409–418Google Scholar
  36. 36.
    Chandler PM and Robertson M (1994) Gene expression regulated by abscisic acid and its relation to stress tolerance. Ann Rev Plant Physiol Plant Mol Biol 45: 113–141Google Scholar
  37. 37.
    Chauvin L-P, Houde M and Sarhan F (1993) A leaf-specific gene stimulated by light during wheat acclimation to low temperature. Plant Mol Biol 23: 255–265Google Scholar
  38. 38.
    Chauvin L-P, Houde M and Sarhan F (1994) Nucleotide sequence of a new member of the freezing tolerance associated protein family in wheat. Plant Physiol 105: 1017–1018Google Scholar
  39. 39.
    Chen PM, Burke MJ and Li PH (1976) The frost hardiness of several Solanum species in relation to the freezing of water, melting point depression, and tissue water content. Bot Gaz 137: 313–317Google Scholar
  40. 40.
    Chu B, Snusted P and Carter JV (1993) Alterations of β-tubulin gene expression during low-temperature exposure in leaves of Arabidopsis thaliana. Plant Physiol 103: 371–377Google Scholar
  41. 41.
    Close TJ (1996) Dehydrins: Emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97: 795–803Google Scholar
  42. 42.
    Close TJ, Meyer NC and Radik J (1995) Nucleotide sequence of a gene encoding a 58.5-kilodalton barley dehydrin that lacks a serine tract. Plant Physiol 107: 289–290Google Scholar
  43. 43.
    Crowe JH, Hoekstra FA and Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54: 570–599Google Scholar
  44. 44.
    Danyluk J. Houde M, Rassart E and Sarhan F (1994) Differential expression of a gene encoding an acidic dehydrin in chilling sensitive and freezing tolerant gramineae species. FEBS Lett 344: 20–24Google Scholar
  45. 45.
    Ding JP and Pickard BG (1993) Modulation of mechanosensitive calcium-selective cation channels by temperature. Plant J 3: 713–720Google Scholar
  46. 46.
    Dörffling K, Dörffling H and Lesselich G (1993) In-vitro selection and regeneration of hydroxyproline-resistant lines of winter-wheat with increased proline content and increased frost tolerance. J Plant Physiol 142: 222–225Google Scholar
  47. 47.
    Dörffling K, Dörffling H, Lesselich G, Luck E, Zimmermann C, Melz G and Jurgens HU (1997) Heritable improvement of frost tolerance in winter wheat by in vitro selection of hydroxyproline-resistant proline overproducing mutants. Euphytica 93: 1–10Google Scholar
  48. 48.
    Droual AM, Maaroufi H, Creche J, Chenieux JC, Rideau M and Hamdi S (1997) Changes in the accumulation of cytosolic cyclophilin transcripts in cultured periwinkle cells following hormonal and stress treatments. J Plant Physiol 151: 142–150Google Scholar
  49. 49.
    Duman JG (1994) Purification and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara. Biochem Biophys Acta 1206: 129–135Google Scholar
  50. 50.
    Duman JG and Olsen TM (1993) Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 30: 322–328Google Scholar
  51. 51.
    Dunn MA, Brown K, Lightolers R and Hughes MA (1996) A low-temperature-responsive gene from barley encodes a protein with single stranded nucleic acid binding activity which is phosphorylated in vitro. PlantMol Biol 30: 947–959Google Scholar
  52. 52.
    Dunn MA, Goddard NJ, Zhang L, Pearce RS and Hughes MA (1994) Low-temperature-responsive barley genes have different control mechanisms. Plant Mol Biol 24: 879–888Google Scholar
  53. 53.
    Dunn MA, Hughes MA, Pearce RS and Jack PL (1990) Molecular characterization of a barley gene induced by cold treatment. J Expt Bot 41: 1405–1413Google Scholar
  54. 54.
    Dunn MA, Hughes MA, Zhang L, Pearce RS, Quigley AS and Jack PL (1991) Nucleotide sequence and molecular analysis of the low-temperature induced cereal gene, blt4. Mol Gen Genet 229: 389–394Google Scholar
  55. 55.
    Dunn MA, Morris A, Jack PL and Hughes MA (1993) A lowtemperature-responsive translation elongation factor 1α from barley (Hordeum vulgare L.). Plant Mol Biol 23: 221–225Google Scholar
  56. 56.
    Dure L III (1993) A repeating 11-mer amino acid motif and plant desiccation. Plant J 3: 363–369Google Scholar
  57. 57.
    Dure L III (1993) Structural motifs in LEA proteins of higher plants. In: Close TJ and Bray EA (eds) Response of Plants to Cellular Dehydration During Environmental Stress. Rockville: American Society of Plant Physiologists, pp 91–103Google Scholar
  58. 58.
    Eagles CF, Williams J and Louis DV (1993) Recovery after freezing in Avena sativa L., Lolium perenne L. and L. multiflorum Lam. New Phytol 123: 477–483Google Scholar
  59. 59.
    Ewart KV, Rubinsky B and Fletcher GL (1994) Structural and functional similarity between fish antifreeze proteins and calcium-dependent lectins. Biochem Biophys Res Commun 185: 335–340Google Scholar
  60. 60.
    Ferullo J-M, Vezina L-P, Rail J, Laberge S, Nadeau P and Castonguay Y (1997) Differential accumulation of two glycine-rich proteins during cold-acclimation of alfalfa. Plant Mol Biol 33: 625–633Google Scholar
  61. 61.
    Fowler DB, Chauvin LP, Limin AE and Sarhan F (1996) The regulatory role of vernalization in the expression of lowtemperature-induced genes in wheat and rye. Theor Appl Genet 93: 554–559Google Scholar
  62. 62.
    Fowler DB, Limin AE, Wang SY and Ward RW (1996) Relationship between low temperature tolerance and vernalization response in wheat and rye. Can J Plant Sci 76: 37–42Google Scholar
  63. 63.
    Franks F (1982) The properties of aqueous solutions at subzero temperatures. In: Franks F (ed) Water: A Comprehensive Treatise, Vol. 7. New York: Plenum Press, pp 215–338Google Scholar
  64. 64.
    Franks F and Hatley RHM (1992) Protein stability under conditions of deep chill. Adv in Low Temp Biol 1: 141–179Google Scholar
  65. 65.
    Galiba G, Kerepesi I, Snape JW and Sutka J (1997) Location of a gene regulating cold-induced carbohydrate production on chromosome 5A of wheat. Theor Appl Genet 95: 265–270Google Scholar
  66. 66.
    Galiba G, Quarrie SA, Sutka J, Morgounov A and Snape JW (1995) RFLP mapping of the vernalization (Vrn1) and frostresistance (Fr1) genes on chromosome 5A of wheat. Theor Appl Genet 90: 1174–1179Google Scholar
  67. 67.
    Gana JA, Sutton F and Kenefick DG (1997) cDNA structure and expression patterns of a low-temperature-specific wheat gene tacr7. Plant Mol Biol 34: 643–650Google Scholar
  68. 68.
    Gaudet DA (1994) Progress towards understanding interaction between cold-hardiness and snow mold resistance and development of resistant cultivars. Can J Plant Pathol 16: 241–246Google Scholar
  69. 69.
    Gibson S, Arondel V, Iba K and Somerville C (1994) Cloning of a temperature-regulated gene encoding a chloroplast ω-3 desaturase from Arabidopsis thaliana. Plant Physiol 106: 1615–1621Google Scholar
  70. 70.
    Gibson S, Falcone DL, Browse J and Somerville C (1994) Use of transgenic plants and mutants to study the regulation and function of lipid composition. Plant, Cell Envir 17: 627–637Google Scholar
  71. 71.
    Gilmour SJ, Artus NN and Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18: 13–21Google Scholar
  72. 72.
    Gilmour SJ and Thomashow MF (1991) Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17: 1233–1240Google Scholar
  73. 73.
    Goday A, Jensen AB, Culianez-Macia FA, Alba MM, Figuerras M, Serratosa J, Torrent M and Pages M (1994) The maize abscisic acid-responsive protein Rab17 is located in the nucleus and interacts with nuclear localization signals. Plant Cell 6: 351–360Google Scholar
  74. 74.
    Goddard NJ, Dunn MA, Zhang L, White AJ, Jack PL and Hughes MA (1993) Molecular analysis and spatial expression pattern of a low-temperature-specific barley gene, blt101. Plant Mol Biol 23: 871–897Google Scholar
  75. 75.
    Godoy J, Lunar R, Torres-Schumann S, Moreno J, Rodrifo RM and Pintor-Toro JA (1994) Expression, tissue distribution and subcellular localization of dehydrin TAS14 in salt-stressed tomato plants. Plant Mol Biol 26: 1921–1934Google Scholar
  76. 76.
    Goodwin W, Pallas JA and Jenkins GI (1996) Transcripts of a gene encoding a putative cell-wall plasma membrane linker protein are specifically cold-induced in Brassica napus. Plant Mol Biol 31: 771–781Google Scholar
  77. 77.
    Gosti F, Bertauche N, Vartanian N and Giraudat J (1995) Abscisic acid-dependent and-independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol Gen Genet 246: 10–18Google Scholar
  78. 78.
    Graham D and Patterson BD (1983) Responses of plants to low, non-freezing temperatures: Proteins, metabolism, and acclimation. Annu Rev Plant Physiol 33: 347–372Google Scholar
  79. 79.
    Gray GR, Chauvin L-P, Sarhan F and Huner NPA (1997) Cold acclimation and freezing tolerance. Plant Physiol 114: 467–474Google Scholar
  80. 80.
    Griffith M, and Antikienen M (1996) Extracellular ice formation in freezing-tolerant plants. Adv Low-Temp Biol 3: 107–139Google Scholar
  81. 81.
    Griffith M, Huner NPA, Espelie KE and Kolattukudy PE (1985) Lipid polymers accumulate in the epidermis and mestome sheath cell walls during low temperature development of winter rye leaves. Protoplasma 125: 53–64Google Scholar
  82. 82.
    Guo W, Ward RW and Thomashow MF (1992) Characterization of a cold-regulated wheat gene related to Arabidopsis cor47. Plant Physiol 100: 915–922Google Scholar
  83. 83.
    Gusta LV, Burke MJ and Kapoor A (1975) Determination of unfrozen water in winter cereals at subfreezing temperatures. Plant Physiol 56: 707–709Google Scholar
  84. 84.
    Guy CL (1990) Cold acclimation and freezing stress tolerance: Role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41: 187–223Google Scholar
  85. 85.
    Guy CL, Huber JLA and Huber SC (1992) Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol 100: 502–508Google Scholar
  86. 86.
    Guy CL, Yelenosky G and Sweet HC (1980) Light exposure and soluble sugars in Citrus frost hardiness. Florida Sci 43: 265–268Google Scholar
  87. 87.
    Hajela RK, Horvath DP, Gilmour SJ and Thomashow MF (1990) Molecular cloning and expression of cor (Cold Regulated) genes in Arabidopsis thaliana. Plant Physiol 93: 1246–1252Google Scholar
  88. 88.
    Hansen J and Beck E (1988) Evidence for ideal and non-ideal equilibrium freezing of leaf water in frosthardy ivy (Hedera helix) and winter barley (Hordeum vulgare). Bot Acta 101: 76–82Google Scholar
  89. 89.
    Harris P and James AT (1969) The effect of low temperatures on fatty acid biosynthesis in plants. Biochem J 112: 325–330Google Scholar
  90. 90.
    Harrison LC, Weiser CJ and Burke MJ (1978) Freezing of water in red osier dogwood stems in relation to cold hardiness. Plant Physiol 62: 899–901Google Scholar
  91. 91.
    Hayashi H, Alia, Mustardy L, Ida M and Murata N (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J 12: 133–142Google Scholar
  92. 92.
    Hayes PM, Blake T, Chen THH, Tragoonrung S, Chen F, Pan A and Liu B (1993) Quantitative trait loci on barley (Hordeum vulgare L) chromosome 7 associated with components of winter hardiness. Genome 36: 66–71Google Scholar
  93. 93.
    Hincha DK, Meins F and Schmitt JM (1997) beta-1,3-glucanase is cryoprotective in vitro and is accumulated in leaves during cold acclimation. Plant Physiol 114: 1077–1083Google Scholar
  94. 94.
    Holoppa LD and Walker-Simmons MK (1995) The wheat abscisic acid-responsive protein-kinase messenger-RNA, PKABA1, is up-regulated by dehydration, cold temperature, and osmotic-stress. Pllant Physiol 108: 1203–1210Google Scholar
  95. 95.
    Hon W-C, Griffith M, Chong P and Yang DSC (1994) Extraction and isolation of antifreeze proteins from winter rye (Secale cereale L.) leaves. Plant Physiol 104: 971–980Google Scholar
  96. 96.
    Hon W-C, Griffith M, Mlynarz A, Zhang J and Yang DSC (1994) The Dual Role of Antifreeze Proteins in Winter Rye. Abstracts, Fourth International Congress of Plant Molecular Biology, Session 10-6; Abstract No. 1979Google Scholar
  97. 97.
    Hong SW, Jon JH, Kwak JM and Nam HG (1997) Identification of a receptor-like protein kinase gene rapidly induced by abscisic acid, dehydration, high salt, and cold treatments in Arabidopsis thaliana. Plant Physiol 113: 1203–1212Google Scholar
  98. 98.
    Horvath D, McLarney BK and Thomashow MF (1993) Regulation of Arabidopsis thaliana L. (Heyn) cor78 in response to low temperature. Plant Physiol 103: 1047–1053Google Scholar
  99. 99.
    Houde M, Daniel C, Lachapelle M, Allard F, Laliberté S, and Sarhan F (1995) Immunolocalisation of freezing-tolerance associated proteins in the cytoplasm and nucleoplasm of wheat crown tissues. Plant J 8: 583–593Google Scholar
  100. 100.
    Houde M, Danyluk J, Laliberte JF, Rassart E, Dhindsa RS and Sarhan F (1992) Cloning, characterization, and expression of a carrier DNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol 99: 1381–1387Google Scholar
  101. 101.
    Houde M, Dhindsa RS and Sarhan F (1992) A molecular marker to select for freezing tolerance in Gramineae. Mol Gen Gen 234: 43–48Google Scholar
  102. 102.
    Hughes MA and Dunn MA (1996) The molecular biology of plant acclimation to low temperature. J Exp Bot 47: 291–305Google Scholar
  103. 103.
    Hughes MA, Dunn MA, Pearce RS, White AJ and Zhang L (1992) An abscisic acid-responsive, low temperature barley gene has homology with a maize phospholipid transfer protein. Plant Cell Envir 15: 861–865Google Scholar
  104. 104.
    Hughes MA and Pearce RS (1988) Low temperature treatment of barley plants causes altered gene expression in leaf meristems. J Exp Bot 39: 1461–1467Google Scholar
  105. 105.
    Hull MR, Long SP and Jahnke LS (1997) Instantaneous and developmental effects of low temperature on the catalytic properties of antioxidant enzymes in two Zea species. Aust J Plant Physiol 24: 337–343Google Scholar
  106. 106.
    Igarashi Y, Yoshiba Y, Sanada Y, Yamaguchi Shinozaki K, Wada K and Shinozaki K (1997) Characterisation of the gene for Delta(1)-pyrroline-5-carboxylate synthase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant Mol Biol 33: 857–865Google Scholar
  107. 107.
    Ishikawa M and Sakai A (1985) Extraorgan freezing in winter flower buds of Cornus officinalis Sieb. Et Zucc. Plant Cell Envir 8: 333–338Google Scholar
  108. 108.
    Ishitani M, Xiong L, Stevenson B and Zhu J-K (1997) Genetic analysis of osmotic stress signal transduction in Arabidopsis: Interactions and convergence of abscisic aciddependent and abscisic acid-independent pathways. Plant Cell 9: 1935–1949Google Scholar
  109. 109.
    Ishizaki-Nishizawa O, Fujii T, Azuma M, Sekiguchi K, Murata N, Ohtani T and Toguri I (1996) Low temperature resistance of higher plants is significantly enhanced by a nonspecific cyanobacterial desaturase. Nature Biotech 14: 1003–1006Google Scholar
  110. 110.
    Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O and Thomashow MF (1998) Arabidopsis CBF1 over expression induces COR genes and enhances freezing tolerance. Science 280: 104–106Google Scholar
  111. 111.
    Jahnke LS, Hull MR and Long SP (1991) Chilling stress and oxygen metabolizing enzymes in Zea mays and Zea diploperennis. Plant Cell Envir 14: 97–104Google Scholar
  112. 112.
    Jarillo JA, Capel J, Leyva A, Martinez-Zapater JM and Salinas J (1994) 2 related low-temperature-inducible genes of Arabidopsis encode proteins showing high homology to 14-3-3 proteins, a family of putative kinase regulators. Plant Mol Biol 25: 693–704Google Scholar
  113. 113.
    Jarillo JA, Leyva A, Salinas J and Martinez-Zapater JM (1993) Low temperature induces the accumulation of alcohol dehydrogenase mRNA in Arabidopsis thaliana, a chillingtolerant plant. Plant Physiol 101: 833–837Google Scholar
  114. 114.
    Kader J-C (1996) Lipid-transfer proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 627–654Google Scholar
  115. 115.
    Kazuoka T and Oeda K (1994) Purification and characterization of COR85-oligomeric complex from cold-acclimation spinach. Plant Cell Physiol 35: 601–611Google Scholar
  116. 116.
    Kirch HH, vanBerkel J, Glaczinski H, Salamini F and Gebhardt C (1997) Structural organisation, expression and promoter activity of a cold-stress-inducible gene of potato (Solanum tuberosum L). Plant Mol Biol 33: 897–909Google Scholar
  117. 117.
    Kitaura K (1967) Freezing and injury of mulberry trees by late spring frost. Bull Sericult Exp Stn (Tokyo) 22: 202–323Google Scholar
  118. 118.
    Knight MR, Campbell AK, Smith SM and Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch, cold-shock and elicitors on cytoplasmic calcium. Nature 352: 524–526Google Scholar
  119. 119.
    Knight H, Trewavas AJ and Knight MR (1996) Cold calcium signalling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8: 489–503Google Scholar
  120. 120.
    Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 509–540Google Scholar
  121. 121.
    Krivosheeva A, Tao DL, Ottander C, Wingsle G, Dube SL and Öoquist G (1996) Cold-acclimation and photoinhibition of photosynthesis in Scots pine. Planta 200: 296–305Google Scholar
  122. 122.
    Kurkela S and Borg-Franck M (1992) Structure and expression of kin2, one of two cold-and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol 19: 689–692Google Scholar
  123. 123.
    Kurkela S and Franck M (1990) Cloning and characterization of a cold-and ABA-inducible Arabidopsis gene. Plant Mol Biol 15: 137–144Google Scholar
  124. 124.
    Laberge S, Castonguay Y and Vezina L-P (1993) New coldand drought-regulated gene from Medicago sativa. Plant Physiol 101: 1411–1412Google Scholar
  125. 125.
    Lång V, Mäntyla E, Welin B, Sundberg B and Palva ET (1994) Alterations in water status, endogenous abscisic acid content and expression of rab18 gene during the development of freezing tolerance in Arabidopsis thaliana (L.) Heyn. Plant Physiol 104: 1341–1349Google Scholar
  126. 126.
    Lång V and Palva ET (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process in Arabidopsis thaliana (L.) Heyn. Plant Mol Biol 20: 951–962Google Scholar
  127. 127.
    Levitt J (1980) Responses of Plants to Environmental Stresses, Vol. 1. New York: Academic Press.Google Scholar
  128. 128.
    Lewis BD, Karlin-Neumann G, Davis RW and Spalding EP (1997) Ca2+-activated anion channels and membrane depolarizations induced by blue light and cold in Arabidopsis seedlings. Plant Physiol 114: 1327–1334Google Scholar
  129. 129.
    Liesenfeld DR, Auld DL, Murray GA and Swensen JB (1986) Transmittance of winterhardiness in segregated populations of peas. Crop Sci 26: 49–54Google Scholar
  130. 130.
    Limin AE, Houde M, Chauvin LP, Fowler DB and Sarhan F (1995) Expression of the cold-induced wheat gene Wcs120 and its homologs in related species and interspecific combinations. Genome 38: 1023–1031Google Scholar
  131. 131.
    Lin C, Guo WW, Everson E and Thomashow MF (1990) Cold acclimation in Arabidopsis thaliana and wheat. Plant Physiol 94: 1078–1083Google Scholar
  132. 132.
    Lin C and Thomashow MF (1992) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene cor15 and characterization of the COR15 polypeptide. Plant Physiol 99: 519–525Google Scholar
  133. 133.
    Lindow SE (1990) Use of genetically altered bacteria to achieve plant frost control. In: Nakas JP and Hagedorn C (eds) Biotechnology of Plant-Microbe Interactions. New York: McGraw-Hill, pp 85–110Google Scholar
  134. 134.
    Lindow SE, Arny PG and Upper CD (1978) Distribution of ice nucleation-active bacteria on plants in nature. App Envir Micro 36: 831–838Google Scholar
  135. 135.
    Lindow SE, Arny PG and Upper CD (1982) Bacterial ice nucleation: A factor in frost injury to plants. Plant Physiol 70: 1084–1089Google Scholar
  136. 136.
    Liu J-J, Galvez AF, Krenz DC and de Lumen BO (1997) Galactinol synthase (GS), a key enzyme in biosynthesis of raffinose family oligosaccharides (RFO): Activation of enzyme activity and induction of gene expression by cold and desiccation. Plant Physiol 114 (supplement): 600Google Scholar
  137. 137.
    Los DA, Horváth I, Vigh L and Murata N (1993) The temperature-dependent expression of the desaturase gene desA in Synechocystis PCC6803. FEBS Lett 318: 57–60Google Scholar
  138. 138.
    Luo M, Lin LH, Hill RD and Mohapatra SS (1991) Primary structure of an environmental stress and abscisic acidinducible alfalfa protein. Plant Mol Biol 17: 1267–1269Google Scholar
  139. 139.
    Luxova M (1986) The hydraulic safety zone at the base of barley roots. Planta 169: 465–470Google Scholar
  140. 140.
    Lynch DV and Steponkus PL (1987) Plasma membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. Cv Puma). Plant Physiol 83: 761–767Google Scholar
  141. 141.
    Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24: 445–466Google Scholar
  142. 142.
    McKersie BD, Bowley SR, Harjanto E and LePrince O (1996) Water-deficit tolerance and field performance of transgenic alfalfa over-expressing superoxide dismutase. Plant Phjysiol 111: 1177–1181Google Scholar
  143. 143.
    McKersie BD, Chen YR, Debeus M, Bowley SR, Bowler C, Inze D, Dhalluin K and Botterman J (1993) Superoxidedismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.). Plant Physiol 103: 1155–1163Google Scholar
  144. 144.
    McKown R, Kuroki G and Warren G (1996) Cold responses of Arabidopsis mutants impaired in freezing tolerance. J Exp Bot 47: 1919–1925Google Scholar
  145. 145.
    Mandal A, Sandgren M, Holmstrom KO, Gallois P and Palva ET (1995) Identification of Arabidopsis thaliana sequences responsive to low-temperature and abscisic-acid by T-DNA tagging and in-vivo gene fusion. PlantMol Biol Rep 13: 243–254Google Scholar
  146. 146.
    Markhart AH, Fiscus EL, Naylor AW and Kramer PJ (1979) Effect of temperature on water and ion transport in soybean and broccoli systems. Plant Physiol 64: 83–87Google Scholar
  147. 147.
    Martin J, Geromanos S, Tempst P and Hartl FU (1993) Identification of nucleotide-binding regions in the chaperonin proteins GroEL and GroES. Nature 366: 279–282Google Scholar
  148. 148.
    Mazur P (1969) Freezing injury in plants. Annu Rev Plant Physiol 20: 419–448Google Scholar
  149. 149.
    Mearns LO, Rosenzweig C and Goldberg R (1992) Effect of changes in interannual climate variability on CERES-wheat yields–sensitivity and 2×CO2 general-circulation model studies. Agric For Met 62: 159–189Google Scholar
  150. 150.
    Meijer EA, de Vries SC, Sterk P, Gadella DWJ, Wirtz KWA and Hendriks T (1993) Characterization of the nonspecific lipid transfer protein–EP2 from carrot (Daucus carota L.). Mol Cell Biochem 123: 159–166Google Scholar
  151. 151.
    Miquel M, James D, Dooner H and Browse J (1993) Arabidopsis requires polyunsaturated lipids for low-temperature survival. Proc Natl Acad Sci USA 90: 6208–6212Google Scholar
  152. 152.
    Mohapatra SS, Wolfraim L, Poole RJ and Dhindsa RS (1989) Molecular cloning and relationship to freezing tolerance of cold-acclimation-specific genes of alfalfa. Plant Physiol 89: 375–380Google Scholar
  153. 153.
    Molina A and García-Olmedo F (1993) Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins. Plant J 4: 983–991Google Scholar
  154. 154.
    Molina A, Mena M, Carbonera P and Garcia-Olmedo F (1997) Differential expression of pathogen-responsive genes encoding two types of glycine-rich proteins in barley. Plant Mol Biol 33: 803–810Google Scholar
  155. 155.
    Molina A, Segura A and García-Olmedo F (1993) Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett 316: 119–122Google Scholar
  156. 156.
    Monroy AF, Castonguay Y, Laberge S, Sarhan F, Vezina LP and Dhindsa RS (1993) A new cold-induced alfalfa gene is associated with enhanced hardening at subzero temperature. Plant Physiol 102: 873–879Google Scholar
  157. 157.
    Monroy AF and Dhindsa RS (1995) Low-temperature signal-transduction–Induction of cold acclimation-specific genes of alfalfa by calcium at 25-degrees-C. Plant Cell 7: 321–331Google Scholar
  158. 158.
    Monroy AF, Sarhan F and Dhindsa RS (1993) Cold-induced changes in freezing tolerance, protein-phosphorylation, and gene-expression–Evidence for a role of calcium. Plant Physiol 102: 1227–1235Google Scholar
  159. 159.
    Murata N (1983) Molecular species composition of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Cell Physiol 24: 81–86Google Scholar
  160. 160.
    Murata N, Ishizaki-Nishizawa Q, Higashi S, Hayashi H, Tasaka Y and Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356: 710–713Google Scholar
  161. 161.
    Murata N, Sato N, Takahashi N and Hamazaki Y (1982) Composition and positional distribution of fatty acids in phospholipids from leaves of chilling-sensitive and chilling-resistant plants. Plant Cell Physiol 23: 1071–1079Google Scholar
  162. 162.
    Ndong C, Ouellet F, Houde M and Sarhan F (1997) Gene expression during cold acclimation in strawberry. Plant Cell Physiol 38: 863–870Google Scholar
  163. 163.
    Neven LG, Haskell DW, Hofig A, Li Q-B and Guy CL (1993) Characterisation of a spinach gene responsive to low temperatures and water stress. Plant Mol Biol 21: 291–305Google Scholar
  164. 164.
    Ng NFL and Hew CL (1992) Structure of an antifreeze polypetide from the sea raven. J Biol Chem 267: 16069–16075Google Scholar
  165. 165.
    Nilan RA (1964) The Cytological Genetics of Barley 1951–1962. Monograph Supplement No. 3, Research Studies, Washington State University Press, USAGoogle Scholar
  166. 166.
    Nishida I and Murata N (1996) Chilling sensitivity in plants and cyanobacteria–The critical contribution of membranelipids. Annu Rev Plant Physiol Plant Mol Biol 47: 541–568Google Scholar
  167. 167.
    Nordin K, Heino P and Palva ET (1991) Separate signal pathways regulate the expression of a low-temperature-induced gene in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 16: 1061–1071Google Scholar
  168. 168.
    Nordin K, Vahala T and Palva ET (1993) Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 21: 641–653Google Scholar
  169. 169.
    Olien CR (1964) Freezing processes in the crown of Hudson barley, Hordeum vulgare (L. emend. Lam.) Hudson. Crop Sci 4: 91–95Google Scholar
  170. 170.
    Olien CR (1967) Freezing stresses and survival. Annu Rev Plant Physiol 18: 387–408Google Scholar
  171. 171.
    Olien CR and Smith MN (1977) Ice adhesions in relation to freeze stress. Plant Physiol 60: 499–503Google Scholar
  172. 172.
    Ouellet F, Houde M and Sarhan F (1993) Purification, characterization and cDNA cloning of the 299 kDa protein induced by cold acclimation in wheat. Plant Cell Physiol 34: 59–65Google Scholar
  173. 173.
    Pan A, Hayes PM, Chen F, Chen THH, Blake T, Wright S, Karsai I and Bedö Z (1994) Genetic analysis of the components of winter hardiness in barley (Hordeum vulgare L). Theor Appl Genet 89: 900–910Google Scholar
  174. 174.
    Parswell DA and Lindquist S (1993) The function of heatshock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Ann Rev Genet 27: 437–496Google Scholar
  175. 175.
    Pearce RS (1985) A freeze-fracture study of membranes of rapidly drought-stressed leaf bases of wheat. J Exp Bot 36: 1209–1221Google Scholar
  176. 176.
    Pearce RS (1985) The membranes of slowly drought-stressed wheat seedlings: A freeze fracture study. Planta 166: 1–14Google Scholar
  177. 177.
    Pearce RS (1988) Extracellular ice and cell shape in frosts-tressed cereal leaves: A low temperature scanning electron microscopy study. Planta 175: 313–324Google Scholar
  178. 178.
    Pearce RS and Ashworth EN (1992) Cell shape and localization of ice in leaves of overwintering wheat during frost stress in the field. Planta 188: 324–331Google Scholar
  179. 179.
    Pearce RS, Dunn MA and Hughes MA (1993) Molecular biology of cold tolerance. In: Jackson MB and Black CR (eds) Interacting Stresses on Plants in a Changing Climate; NATO ASI Series I: Global Environmental Change, Vol. 16. Berlin: Springer, pp. 681–695Google Scholar
  180. 180.
    Pearce RS, Dunn MA, Rixon JE, Harrison P and Hughes MA (1996) Expression of cold-induced genes and frost hardiness in the crown meristem of young barley (Hordeum vulgare L. cv. Igri) plants grown in different environments. Plant Cell & Envir 12: 275–290Google Scholar
  181. 181.
    Pearce RS, Houlston CE, Atherton KA, Rixon JE, Harrison P, Hughes MA and Dunn MA(1998) Localization of expression of three cold-induced genes (blt101, blt4.9, blt14) in different tissues of the crown and developing leaves of cold-acclimated cultivated barley (Hordeum vulgare L. cv. Igri). Plant Physiol 117: 787–795Google Scholar
  182. 182.
    Pearce RS and Willison JHM (1985) Wheat tissues freeze-etched during exposure to extracellular freezing: Distribution of ice. Planta 163: 295–303Google Scholar
  183. 183.
    Pearce RS and Willison JHM (1985) A freeze-etch study of the effect of extracellular freezing on the cellular membranes of wheat. Planta 163: 304–316Google Scholar
  184. 184.
    Phillips JR, Dunn MA and Hughes MA (1997) mRNA stability and localisation of the low-temperature-responsive barley gene family blt14. Plant Mol Biol 33: 1013–1023Google Scholar
  185. 185.
    Pihakaski-Maunsbach K, Griffiths M, Antikainen M and Maunsbach AB (1996) Immunogold localization of glucanase-like antifreeze protein in cold acclimated winter rye. Protoplasma 191: 115–125Google Scholar
  186. 186.
    Plant AL, Cohen A, Moses MS and Bray EA (1997) Nucleotide sequence and spatial expression pattern of a droughtand abscisic acid-induced gene of tomato. Plant Physiol 97: 900–906Google Scholar
  187. 187.
    Polinsky DH and Braam J (1996) Cold-shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels. Plant Physiol 111: 1271–1279Google Scholar
  188. 188.
    Pollock CJ and Jones T (1979) Seasonal patterns of fructan metabolism in forage grasses. New Phytol 83: 8–15Google Scholar
  189. 189.
    Prasad TK (1997) Role of catalase in inducing chilling tolerance in pre-emergent maize seedlings. Plant Physiol 114: 1369–1376Google Scholar
  190. 190.
    Prasad TK, Anderson MD, Martin BA and Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6: 65–74Google Scholar
  191. 191.
    Pyee J, Yu H and Kolattukudy PE (1994) Identification of a lipid transfer protein as the major protein in the surface wax of broccoli (Brassica oleracea) leaves. Arch Biochem Biophys 311: 460–468Google Scholar
  192. 192.
    Rajashekar CB and Burke MJ (1982) Liquid water during slow freezing based on cell water relations and limited experimental testing. In: Li PH and Sakai A (eds) Plant Cold Hardiness and Freezing Stress, Vol. 2. New York: Academic Press, pp 211–220Google Scholar
  193. 193.
    Rebeille F, Bligny R and Douce R (1980) Oxygen and temperature effects on the fatty acid composition of sycamore cells (Acer pseudoplatanus L.). Biochem. Biophys. Acta 620: 1–9Google Scholar
  194. 194.
    Reimholz R, Geiger M, Haake V, Deiting U, Krause KP, Sonnewald U and Stitt M (1997) Potato plants contain multiple forms of sucrose phosphate synthase, which differ in their tissue distributions, their levels during development, and their responses to low temperature. Plant Cell Envir 20: 291–305Google Scholar
  195. 195.
    Roberts DWA (1990) Identification of loci on chromosome 5A of wheat involved in control of cold hardiness, vernalization, leaf length, rosette growth habit, and height of hardened plants. Genome 33: 247–259Google Scholar
  196. 196.
    Robertson AJ, Weninger A, Wilen RW, Fu P and Gusta LV (1994) Comparison of dehydrin gene expression and freezing tolerance in Bromus inermis and Secale cereale grown in controlled environments, hydroponics, and the field. Plant Physiol 106: 1213–1216Google Scholar
  197. 197.
    Rorat T, Irzkowski W and Grygorowicz WJ (1997) Identification and expression of novel cold induced genes in potato (Solanum sogarandinum). Plant Sci 124: 69–78Google Scholar
  198. 198.
    Rouse DT, Marotta A and Parish RW (1996) Promoter and expression studies on an Arabidopsis thaliana dehydrin gene. FEBS Lett 281: 252–256Google Scholar
  199. 199.
    SaezVasquez J, Raynal M, Mezabasso L and Delseny M (1993) 2 related, low-temperature-induced genes from Brassica napus are homologous to the human tumor bbc1 (breast basic conserved) gene. Plant Mol Biol 23: 1211–1221Google Scholar
  200. 200.
    Sakai A (1960) Survival of twigs of woody plants at —196°C. Nature 185: 393–394Google Scholar
  201. 201.
    Sakai A (1962) Survival of woody plants in liquid helium. Low Temp Sci B 20: 121–122Google Scholar
  202. 202.
    Sakai A (1982) Freezing tolerance of shoot and flower primordia of coniferous buds by extraorgan freezing. Plant Cell Physiol 23: 1219–1227Google Scholar
  203. 203.
    Sakai A and Larcher W (1987) Frost Survival of Plants. Berlin: Springer.Google Scholar
  204. 204.
    Salzman RA, Bressan RA, Hasegawa PM, Ashworth EN and Bordelon BP (1996) Programmed accumulation of LEA-like proteins during desiccation and cold-acclimation of overwintering grape buds. Plant Cell Envir 19: 713–720Google Scholar
  205. 205.
    Shibata S and Shimada T (1986) Anatomical observation of the development of freezing injury in orchardgrass crown. J Jap Grass Sci 32: 197–204Google Scholar
  206. 206.
    Sieg F, Schroder W, Schmitt JM and Hincha DK (1996) Purification and characterization of a cryoprotective protein (cryoprotectin) from the leaves of cold-acclimated cabbage. Plant Physiol 111: 215–221Google Scholar
  207. 207.
    Smith H (1990) Signal perception, differential expression within multigene families and the molecular basis of phenotypic plasticity. Plant Cell Envir 13: 585–594Google Scholar
  208. 208.
    Sossountzov l, Riz-Avila L, Vignols F, Jolliot A, Arondel V, Tcheng F, Grosbois M, Guerbette F, Miginiac E, Delseny M, Puigdomenèch M and Kader J-C (1991) Spatial and temporal expression of a maize lipid transfer protein gene. Plant Cell 3: 923–933Google Scholar
  209. 209.
    Steponkus PL and Webb MS (1992) Freeze-induced dehydration and membrane destabilization in plants. In: Somero GN, Osmond CB and Bolis CL (eds) Water and Life: Comparative Analysis of Water Relationships at the Organismic, Cellular and Molecular Level. Berlin: Springer, pp 338–362Google Scholar
  210. 210.
    Steponkus PL (1992) Preface. Advances in Low Temp Biol 1: ix–xiGoogle Scholar
  211. 211.
    Steponkus PL, Uemura M, Balsamo RA, Arvinte T and Lynch DV (1988) Transformation of the cryobehaviour of rye protoplasts by modification of the plasma membrane lipid composition. Proc Natl Acad Sci USA 85: 9026–9030Google Scholar
  212. 212.
    Stockinger EJ, Gilmour EJ and Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domaincontaining transcription activator that binds to the C-repeat/ DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94: 1035–1040Google Scholar
  213. 213.
    Stone JM, Palta JP, Bamberg JB, Weiss LS and Harbage JF (1993) Inheritance of freezing resistance in tuber-bearing Solanum species: Evidence for independent genetic control of nonacclimated freezing tolerance and cold acclimation capacity. Proc Natl Acad Sci USA 90: 7869–7873Google Scholar
  214. 214.
    Strauss G and Hauser H (1986) Stabilization of lipid bilayer vesicles by sucrose during freezing. Proc Natl Acad Sci USA 83: 2422–2426Google Scholar
  215. 215.
    Stushnoff C, Remmele RL, Essensee V and McNeil M (1993) Low temperature induced biochemical mechanisms: Implications for cold acclimation and de-acclimation. In: Jackson MB and Black CR (eds) Interacting Stresses on Plants in a Changing Climate; NATO ASI Series I: Global Environmental Change, Vol. 16. Berlin: Springer, pp 647–657Google Scholar
  216. 216.
    Sutka J (1994) Genetic-control of frost tolerance in wheat (Triticum aestivum L). Euphytica 77: 277–282Google Scholar
  217. 217.
    Sutton F, Ding X and Kenefick DG (1992) Group 3 LEA gene HVA1 regulation by cold acclimation and deacclimation in two barley cultivars with varying freeze resistance. Plant Physiol 99: 338–340Google Scholar
  218. 218.
    Tabaei Aghdaei SR (1997) Studies of Stress Responses in Gramineae (Poaceae) Using Biotechnological Methods. PhD thesis, University of Newcastle upon TyneGoogle Scholar
  219. 219.
    Takahashi R and Shimosaka E (1997) cDNA sequence analysis and expression of two cold-regulated genes in soybean. Plant Sci 123: 93–104Google Scholar
  220. 220.
    Takahashi R and Yasuda S (1970) Genetics of earliness and growth in barley. In: Barley Genetics II. USA: Washington State University Press, pp 388–408Google Scholar
  221. 221.
    Tanino KK and McKersie BD (1985) Injury within the crown of winter wheat seedlings after freezing and icing stress. Can J Bot 63: 432–436Google Scholar
  222. 222.
    Tantau H and Dörffling K (1991) In vitro-selection of hydroxyproline-resistant cell-lines of wheat (Triticumaestivum)–accumulation of proline, decrease in osmotic potential, and increase in frost tolerance. Physiol Plant 82: 243–248Google Scholar
  223. 223.
    Thoma S, Hecht U, Kippers A, Botella J, De Vries S and Somerville C (1994) Tissue-specific expression of a gene encoding a cell wall-localized lipid transfer protein from Arabidopsis. Plant Physiol 105: 35–45Google Scholar
  224. 224.
    Thoma S, Kaneko Y and Somerville C (1993) A non-specific lipid transfer protein from Arabidopsis is a cell wall protein. Plant J 3: 427–436Google Scholar
  225. 225.
    Tiku PE, Gracey AY, Macartney AI, Beynon RJ and Cossins AR (1996) Cold-induced expression of delta(9) desaturase in carp by transcriptional and post-transcriptional mechanisms. Science 271: 815–818Google Scholar
  226. 226.
    Travert S, Valerio L, Fouraste I, Boudet AM and Teulieres C (1997) Enrichment in specific soluble sugars of two Eucalyptus cell-suspension cultures by various treatments enhances their frost tolerance via a noncolligative mechanism. Plant Physiol 114: 1433–1442Google Scholar
  227. 227.
    Tronsmo AM, Gregersen P, Hjeljord L, Sandal T, Brungelsson T and Collinge DB (1993) Cold-induced disease resistance. In: Fritig B and Legrand M (eds) Mechanisms of Plant Defence Responses. Dordrecht: Kluwer Academic Publishers, p 369Google Scholar
  228. 228.
    Tumanov II and Trunova TI (1957) Hardening tissues of winter plants with sugar absorbed from the external solution. Fiziol Rastenii 4: 379–388Google Scholar
  229. 229.
    Uemura M, Joseph RA and Steponkus PL (1995) Coldacclimation of Arabidopsis thaliana–effect on plasmamembrane lipid composition and freeze-induced lesions. Plant Physiol 109: 15–30Google Scholar
  230. 230.
    Uemura M and Steponkus PL (1994) A contrast of the plasma-membrane lipid composition of oat and rye leaves in relation to freezing tolerance. Plant Physiol 104: 479–496Google Scholar
  231. 231.
    Uemura M and Steponkus PL (1997) Effect of cold acclimation on the lipid composition of the inner and outer membrane of the chloroplast envelope isolated from rye leaves. Plant Physiol 114: 1493–1500Google Scholar
  232. 232.
    Van Zee K, Chen FQ, Hayes PM, Close TJ and Chen THH (1995) Cold-specific induction of a dehydrin gene family member in barley. Plant Physiol 108: 1233–1239Google Scholar
  233. 233.
    Veisz O, Galiba G and Sutka J (1996) Effect of abscisic acid on the cold hardiness of wheat seedlings. J Plant Physiol 149: 439–443Google Scholar
  234. 234.
    Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579–620Google Scholar
  235. 235.
    Vigh L, Los Da, Horvath I and Murata (1993) The primary signal in the biological perception of temperature: Pdcatalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803. Proc Natl Acad Sci USA 90: 9090–9094Google Scholar
  236. 236.
    Visick JE and Clarke S (1995) Repair, refold, recycle: How bacteria can deal with spontaneous and environmental damage to proteins. Mol Microbiol 16: 835–845Google Scholar
  237. 237.
    Wallis JG, Wang HY, Guerra DJ (1997) Expression of a synthetic antifreeze protein in potato reduces electrolyte release at freezing temperatures. Plant Mol Biol 35: 323–330Google Scholar
  238. 238.
    Walker MA and McKersie BD (1993) Role of the ascorbateglutathione antioxidant system in chilling resistance of tomato. J Plant Physiol 141: 234–239Google Scholar
  239. 239.
    Warren G, McKown R, Marin A and Teutonica R (1996) Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L) Heynh. Plant Physiol 111: 1011–1019Google Scholar
  240. 240.
    Welin BV, Olson A, Nylander M and Palva ET (1994) Characterization and differential expression of dhn/lea/rablike genes during cold-acclimation and drought stress in Arabidopsis thaliana. Plant Mol Biol 26: 131–144Google Scholar
  241. 241.
    Weretilnyk E, Orr W, White TC, Iu B and Singh J (1993) Characterisation of three related low-temperature-regulated cDNAs from winter Brassica napus. Plant Physiol 101: 171–177Google Scholar
  242. 242.
    White AJ, Dunn AM, Brown K and Hughes MA (1994) Comparative analysis of genomic sequence and expression of a lipid transfer protein gene family in winter barley. J Expt Bot 281: 1885–1892Google Scholar
  243. 243.
    Wilhelm KS and Thomashow MF (1993) Arabidopsis thaliana cor15b, an apparent homologue of cor15a, is strongly responsive to cold and ABA, but not drought. Plant Mol Biol 23: 1073–1077Google Scholar
  244. 244.
    Williams WP (1990) Cold-induced lipid phase transitions. Phil Trans Royal Soc Lond Series B Biol Sci 326: 555–570Google Scholar
  245. 245.
    Williams RJ (1992) Anomalous behaviour of ice in solutions of ice-binding arabinoxylans. Thermochim. Acta 212: 105–113Google Scholar
  246. 246.
    Winter AL, Williams JHH, Thomas DS and Pollock CJ (1994) Changes in gene-expression in response to sucrose accumulation in leaf tissue of Lolium temulentum L. New Phytol 128: 591–600Google Scholar
  247. 247.
    Wisniewski M, Davis G and Arora R (1993) The role of pit membrane structure in deep supercooling of xylem parenchyma. In: Li PH and Christersson L (eds) Advances in Plant Cold Hardiness. Boca Raton, Florida: CRC Press, pp 215–228Google Scholar
  248. 248.
    Wisniewski M, Davis G and Schaffer K (1991) Mediation of deep supercooling of peach and dogwood by enzymatic modification in cell-wall structure. Planta 184: 254–260Google Scholar
  249. 249.
    Wolfraim LA and Dhindsa RS (1993) Cloning and sequencing of the cDNA for cas17, a cold acclimation-specific gene of alfalfa. Plant Physiol 103: 667–668Google Scholar
  250. 250.
    Wolfraim LA, Langis R, Tyson H and Dhindsa RS (1993) cDNA sequence, expression, and transcript stability of a cold acclimation-specific gene, cas18, of alfalfa (Medicago falcata) cells. Plant Physiol 101: 1275–1282Google Scholar
  251. 251.
    Wolter F-P, Schmidt R and Heinz E (1992) Chilling sensitivity of Arabidopsis thaliana with genetically engineered membrane lipids. EMBO J 11: 4685–4692Google Scholar
  252. 252.
    Worland AJ, Gale MD and Law CN (1987) Wheat genetics. In: Lupton FGH (ed) Wheat Breeding. London, UK: Chapman and Hall, pp 129–171Google Scholar
  253. 253.
    Wu JR and Browse J (1995) Elevated levels of high-melting point phosphatidyl glycerols do not induce chilling sensitivity in an Arabidopsis mutant. Plant Cell 7: 17–27Google Scholar
  254. 254.
    Xu W, Cambell P, Vargheese AK and Braam J (1996) The Arabidopsis XET-related gene family–Environmental regulation and hormonal regulation of expression. Plant J 9: 879–889Google Scholar
  255. 255.
    Xu DP, Duan XL, Wang BY, Hong BM, Ho THD and Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110: 249–257Google Scholar
  256. 256.
    Yamaguchi-Shinozaki K and Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 251–264Google Scholar
  257. 257.
    Zamecník J, BieblovaáJ and Grospietch M (1994) Safety zone as a barrier to root-shoot ice propagation. Plant and Soil 167: 149–155Google Scholar
  258. 258.
    Zhang L, Dunn MA, Pearce RS and Hughes MA (1993) Analysis of organ specificity of a low temperature responsive gene family in rye (Secale cereale L). J Exp Bot 44: 1787–1793Google Scholar
  259. 259.
    Zhang H, Wang J, Nickel U, Allen RD and Goodman HM (1997) Cloning and expression of an Arabidopsis gene encoding a putative peroxisomal ascorbate peroxidase. Plant Mol Biol 34: 967–971Google Scholar
  260. 260.
    Zhu J-J and Beck E (1991) Water relations of Pachysandra leaves during freezing and thawing. Plant Physiol 97: 1146–1153Google Scholar
  261. 261.
    Zhu B, Chen THH and Li PH (1993) Expression of an ABA-responsive osmotin-like gene during the induction of freezing tolerance in Solanum commersonii. Plant Mol Biol 21: 729–735Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Roger S. Pearce
    • 1
  1. 1.Department of Biological and Nutritional SciencesThe UniversityNewcastle upon TyneUK (Phone

Personalised recommendations